Fates of acid-resistant and non-acid-resistant Shiga toxin-producing Escherichia coli strains in ruminant digestive contents in the absence and presence of probiotics

Abstract

Healthy ruminants are the main reservoir of Shiga toxin-producing Escherichia coli (STEC). During their transit through the ruminant gastrointestinal tract, STEC encounters a number of acidic environments. As all STEC strains are not equally resistant to acidic conditions, the purpose of this study was to investigate whether acid resistance confers an ecological advantage to STEC strains in ruminant digestive contents and whether acid resistance mechanisms are induced in the rumen compartment. We found that acid-resistant STEC survived at higher rates during prolonged incubation in rumen fluid than acid-sensitive STEC and that they resisted the highly acidic conditions of the abomasum fluid, whereas acid-sensitive strains were killed. However, transit through the rumen contents allowed acid-sensitive strains to survive in the abomasum fluid at levels similar to those of acid-resistant STEC. The acid resistance status of the strains had little influence on STEC growth in jejunal and cecal contents. Supplementation with the probiotic Saccharomyces cerevisiae CNCM I-1077 or Lactobacillus acidophilus BT-1386 led to killing of all of the strains tested during prolonged incubation in the rumen contents, but it did not have any influence in the other digestive compartments. In addition, S. cerevisiae did not limit the induction of acid resistance in the rumen fluid. Our results indicate that the rumen compartment could be a relevant target for intervention strategies that could both limit STEC survival and eliminate induction of acid resistance mechanisms in order to decrease the number of viable STEC cells reaching the hindgut and thus STEC shedding and food contamination.

FIG. 1.

Survival of STEC strains in the rumen fluid. Three independent experiments were performed. (A) STEC survival rates after 24 h of incubation. (B) STEC survival curves. A representative curve is shown for each strain.

FIG. 2.

STEC survival rates after 1.5 h of incubation in the abomasal fluid. Three independent experiments were performed.

FIG. 3.

Growth of STEC strains in jejunal (A) and cecal (B) contents. Three independent experiments were performed.

FIG. 4.

Influence of 6 h of preincubation in rumen contents on the survival of STEC strains in the abomasum fluid. Solid lines and dotted lines indicate the survival of STEC in the abomasum without preincubation and after preincubation (P), respectively. (A) Preincubation in the rumen contents of grain- and hay-fed animals. (B) Preincubation in the rumen contents of hay-fed animals. Three independent experiments were performed. A representative curve is shown for each strain.

FIG. 5.

Effect of probiotics on EDL933 survival in the rumen fluid. Control, EDL933 survival without probiotics; SC, EDL933 survival in the rumen fluid in the presence of S. cerevisiae; LA, EDL933 survival in the rumen fluid in the presence of L. acidophilus. Three independent experiments were performed. A representative curve is shown for each condition.